Gamma delta T cells are activated by polysaccharide K (PSK) and contribute to the anti-tumor effect of PSK

Cancer Immunology, Immunotherapy

Volumn 62, Issue 8, 2013, Pages 1335-1345

  Inatsuka, Carol ^a   Yang, Yi ^a   Gad, Ekram ^a   Rastetter, Lauren ^a   Disis, Mary L ^a   Lu, Hailing ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

T cells; Breast cancer; Innate immunity; Polysaccharide; PSK; TLR

Indexed keywords

CD69 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 2 RECEPTOR ALPHA; KRESTIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; TOLL LIKE RECEPTOR 2;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG MECHANISM; GAMMA DELTA T LYMPHOCYTE; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; T LYMPHOCYTE ACTIVATION; TUMOR ASSOCIATED LEUKOCYTE; UPREGULATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD3; ANTINEOPLASTIC AGENTS; BONE MARROW CELLS; CELL COMMUNICATION; CELL LINE, TUMOR; CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITIC CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; FLOW CYTOMETRY; INTERFERON-GAMMA; LYMPHOCYTE ACTIVATION; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED STRAINS; MICE, TRANSGENIC; PROTEOGLYCANS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; SPLEEN; T-LYMPHOCYTES; TUMOR BURDEN;

EID: 84880923112     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-013-1436-4     Document Type: Article

References (46)

1. Ernst E, Cassileth BR (1998) The prevalence of complementary/alternative medicine in cancer: a systematic review. Cancer 83:777-782. doi: 10.1002/(SICI)1097-0142(19980815)83:4<777:AID-CNCR22>3.0.CO;2-O
2. Cassileth BR, Vickers AJ (2005) High prevalence of complementary and alternative medicine use among cancer patients: implications for research and clinical care. J Clin Oncol 23:2590-2592. doi: 10.1200/JCO.2005.11.922
3. Hyodo I, Amano N, Eguchi K, Narabayashi M, Imanishi J, Hirai M, Nakano T, Takashima S (2005) Nationwide survey on complementary and alternative medicine in cancer patients in Japan. J Clin Oncol 23:2645-2654. doi: 10.1200/JCO.2005.04.126
4. Kidd PM (2000) The use of mushroom glucans and proteoglycans in cancer treatment. Altern Med Rev 5:4-27
5. Fisher M, Yang LX (2002) Anticancer effects and mechanisms of polysaccharide-K (PSK): implications of cancer immunotherapy. Anticancer Res 22:1737-1754
6. Sakamoto J, Morita S, Oba K, Matsui T, Kobayashi M, Nakazato H, Ohashi Y (2006) Efficacy of adjuvant immunochemotherapy with polysaccharide K for patients with curatively resected colorectal cancer: a meta-analysis of centrally randomized controlled clinical trials. Cancer Immunol Immunother 55:404-411
7. Lu H, Yang Y, Gad E et al (2011) Polysaccharide krestin is a novel TLR2 agonist that mediates inhibition of tumor growth via stimulation of CD8 T cells and NK cells. Clin Cancer Res 17:67-76. doi: 10.1158/1078-0432.CCR-10-1763
8. Kabelitz D, Wesch D, He W (2007) Perspectives of gammadelta T cells in tumor immunology. Cancer Res 67:5-8
9. Groh V, Rhinehart R, Secrist H, Bauer S, Grabstein KH, Spies T (1999) Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci USA 96:6879-6884
10. Girardi M, Oppenheim DE, Steele CR et al (2001) Regulation of cutaneous malignancy by gammadelta T cells. Science 294:605-609. doi: 10.1126/science. 1063916
11. Liu Z, Eltoum IE, Guo B, Beck BH, Cloud GA, Lopez RD (2008) Protective immunosurveillance and therapeutic antitumor activity of gammadelta T cells demonstrated in a mouse model of prostate cancer. J Immunol 180:6044-6053
12. Gao Y, Yang W, Pan M, Scully E, Girardi M, Augenlicht LH, Craft J, Yin Z (2003) Gamma delta T cells provide an early source of interferon gamma in tumor immunity. J Exp Med 198:433-442. doi: 10.1084/jem.20030584
13. Kobayashi H, Tanaka Y, Yagi J, Osaka Y, Nakazawa H, Uchiyama T, Minato N, Toma H (2007) Safety profile and anti-tumor effects of adoptive immunotherapy using gamma-delta T cells against advanced renal cell carcinoma: a pilot study. Cancer Immunol Immunother 56:469-476. doi: 10.1007/s00262-006-0199-6
14. Nicol AJ, Tokuyama H, Mattarollo SR, Hagi T, Suzuki K, Yokokawa K, Nieda M (2011) Clinical evaluation of autologous gamma delta T cell-based immunotherapy for metastatic solid tumours. Br J Cancer 105:778-786. doi: 10.1038/bjc.2011.293
15. Lopez RD, Xu S, Guo B, Negrin RS, Waller EK (2000) CD2-mediated IL-12-dependent signals render human gamma delta-T cells resistant to mitogen-induced apoptosis, permitting the large-scale ex vivo expansion of functionally distinct lymphocytes: implications for the development of adoptive immunotherapy strategies. Blood 96:3827-3837
16. Mattarollo SR, Kenna T, Nieda M, Nicol AJ (2007) Chemotherapy and zoledronate sensitize solid tumour cells to Vgamma9 Vdelta2 T cell cytotoxicity. Cancer Immunol Immunother 56:1285-1297. doi: 10.1007/s00262-007-0279-2
17. Dieli F, Vermijlen D, Fulfaro F et al (2007) Targeting human gamma}delta T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res 67:7450-7457
18. Beck BH, Kim HG, Kim H, Samuel S, Liu Z, Shrestha R, Haines H, Zinn K, Lopez RD (2010) Adoptively transferred ex vivo expanded gammadelta-T cells mediate in vivo antitumor activity in preclinical mouse models of breast cancer. Breast Cancer Res Treat 122:135-144. doi: 10.1007/s10549-009-0527-6
19. Hannani D, Ma Y, Yamazaki T, Dechanet-Merville J, Kroemer G, Zitvogel L (2012) Harnessing gammadelta T cells in anticancer immunotherapy. Trends Immunol 33:199-206. doi: 10.1016/j.it.2012.01.006
20. Wesch D, Peters C, Oberg HH, Pietschmann K, Kabelitz D (2011) Modulation of gammadelta T cell responses by TLR ligands. Cell Mol Life Sci 68:2357-2370. doi: 10.1007/s00018-011-0699-1
21. Lu H, Knutson KL, Gad E, Disis ML (2006) The tumor antigen repertoire identified in tumor-bearing Neu transgenic mice predicts human tumor antigens. Cancer Res 66:9754-9761
22. Knutson KL, Lu H, Stone B, Reiman JM, Behrens MD, Prosperi CM, Gad EA, Smorlesi A, Disis ML (2006) Immunoediting of cancers may lead to epithelial to mesenchymal transition. J Immunol 177:1526-1533
23. Lu H, Yang Y, Gad E, Inatsuka C, Wenner CA, Disis ML, Standish LJ (2011) TLR2 agonist PSK activates human NK cells and enhances the antitumor effect of HER2-targeted monoclonal antibody therapy. Clin Cancer Res 17:6742-6753. doi: 10.1158/1078-0432.CCR-11-1142
24. Jimenez E, Garcia-Lora A, Martinez M, Garrido F (2005) Identification of the protein components of protein-bound polysaccharide (PSK) that interact with NKL cells. Cancer Immunol Immunother 54:395-399. doi: 10.1007/s00262-004-0601-1
25. Deetz CO, Hebbeler AM, Propp NA, Cairo C, Tikhonov I, Pauza CD (2006) Gamma interferon secretion by human Vgamma2 Vdelta2 T cells after stimulation with antibody against the T-cell receptor plus the Toll-Like receptor 2 agonist Pam3Cys. Infect Immun 74:4505-4511
26. Oba K, Teramukai S, Kobayashi M, Matsui T, Kodera Y, Sakamoto J (2007) Efficacy of adjuvant immunochemotherapy with polysaccharide K for patients with curative resections of gastric cancer. Cancer Immunol Immunother 56:905-911. doi: 10.1007/s00262-006-0248-1
27. Torisu M, Hayashi Y, Ishimitsu T et al (1990) Significant prolongation of disease-free period gained by oral polysaccharide K (PSK) administration after curative surgical operation of colorectal cancer. Cancer Immunol Immunother 31:261-268
28. Dunn GP, Koebel CM, Schreiber RD (2006) Interferons, immunity and cancer immunoediting. Nat Rev Immunol 6:836-848
29. Trinchieri G (2003) Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 3:133-146. doi: 10.1038/nri1001
30. Devilder MC, Allain S, Dousset C, Bonneville M, Scotet E (2009) Early triggering of exclusive IFN-gamma responses of human Vgamma9Vdelta2 T cells by TLR-activated myeloid and plasmacytoid dendritic cells. J Immunol 183:3625-3633. doi: 10.4049/jimmunol.0901571
31. Kunzmann V, Kretzschmar E, Herrmann T, Wilhelm M (2004) Polyinosinic-polycytidylic acid-mediated stimulation of human gammadelta T cells via CD11c dendritic cell-derived type I interferons. Immunology 112:369-377. doi: 10.1111/j.1365-2567.2004.01908.x
32. Nedellec S, Sabourin C, Bonneville M, Scotet E (2010) NKG2D costimulates human V gamma 9V delta 2 T cell antitumor cytotoxicity through protein kinase C theta-dependent modulation of early TCR-induced calcium and transduction signals. J Immunol 185:55-63. doi: 10.4049/jimmunol.1000373
33. Das H, Groh V, Kuijl C, Sugita M, Morita CT, Spies T, Bukowski JF (2001) MICA engagement by human Vgamma2Vdelta2 T cells enhances their antigen-dependent effector function. Immunity 15:83-93
34. Groh V, Steinle A, Bauer S, Spies T (1998) Recognition of stress-induced MHC molecules by intestinal epithelial gammadelta T cells. Science 279:1737-1740
35. Hamerman JA, Ogasawara K, Lanier LL (2004) Cutting edge: toll-like receptor signaling in macrophages induces ligands for the NKG2D receptor. J Immunol 172:2001-2005
36. Kloss M, Decker P, Baltz KM, Baessler T, Jung G, Rammensee HG, Steinle A, Krusch M, Salih HR (2008) Interaction of monocytes with NK cells upon Toll-like receptor-induced expression of the NKG2D ligand MICA. J Immunol 181:6711-6719
37. Eissmann P, Evans JH, Mehrabi M, Rose EL, Nedvetzki S, Davis DM (2010) Multiple mechanisms downstream of TLR-4 stimulation allow expression of NKG2D ligands to facilitate macrophage/NK cell crosstalk. J Immunol 184:6901-6909. doi: 10.4049/jimmunol.0903985
38. Pietschmann K, Beetz S, Welte S, Martens I, Gruen J, Oberg HH, Wesch D, Kabelitz D (2009) Toll-like receptor expression and function in subsets of human gammadelta T lymphocytes. Scand J Immunol 70:245-255. doi: 10.1111/j.1365-3083. 2009.02290.x
39. Martin B, Hirota K, Cua DJ, Stockinger B, Veldhoen M (2009) Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals. Immunity 31:321-330. doi: 10.1016/j.immuni.2009.06.020
40. Hedges JF, Lubick KJ, Jutila MA (2005) Gamma delta T cells respond directly to pathogen-associated molecular patterns. J Immunol 174:6045-6053
41. Reynolds JM, Martinez GJ, Chung Y, Dong C (2012) Toll-like receptor 4 signaling in T cells promotes autoimmune inflammation. Proc Natl Acad Sci USA 109:13064-13069. doi: 10.1073/pnas.1120585109
42. Kamath AB, Wang L, Das H, Li L, Reinhold VN, Bukowski JF (2003) Antigens in tea-beverage prime human Vgamma 2Vdelta 2 T cells in vitro and in vivo for memory and nonmemory antibacterial cytokine responses. Proc Natl Acad Sci USA 100:6009-6014
43. Holderness J, Schepetkin IA, Freedman B, Kirpotina LN, Quinn MT, Hedges JF, Jutila MA (2011) Polysaccharides isolated from Acai fruit induce innate immune responses. PLoS ONE 6:e17301. doi: 10.1371/journal.pone.0017301
44. Graff JC, Kimmel EM, Freedman B, Schepetkin IA, Holderness J, Quinn MT, Jutila MA, Hedges JF (2009) Polysaccharides derived from Yamoa (Funtumia elastica) prime gammadelta T cells in vitro and enhance innate immune responses in vivo. Int Immunopharmacol 9:1313-1322. doi: 10.1016/j.intimp.2009.07.015
45. Deng G, Lin H, Seidman A et al (2009) A phase I/II trial of a polysaccharide extract from Grifola frondosa (Maitake mushroom) in breast cancer patients: immunological effects. J Cancer Res Clin Oncol 135:1215-1221. doi: 10.1007/s00432-009-0562-z
46. Torkelson CJ, Sweet E, Martzen MR, Sasagawa M, Wenner CA, Gay J, Putiri A, Standish LJ (2012) Phase 1 clinical trial of trametes versicolor in women with breast cancer. ISRN Oncol 2012:251632. doi: 10.5402/2012/251632